Identification of Mn(II)-oxidizing bacteria from a Low-pH contaminated former uranium mine

Applied and Environmental Microbiology

Volumn 80, Issue 16, 2014, Pages 5086-5097

  Akob, Denise M ^a,b   Bohu, Tsing ^a   Beyer, Andrea ^a   Schäffner, Franziska ^a   Händel, Matthias ^a   Johnson, Carol A ^c   Merten, Dirk ^a   Büchel, Georg ^a   Totsche, Kai Uwe ^a   Küsel, Kirsten ^a,d  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b U S GEOLOGICAL SURVEY   (United States)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^d GERMAN CENTRE FOR INTEGRATIVE BIODIVERSITY RESEARCH IDIV HALLE JENA LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CADMIUM; OXIDATION; SOILS; STRAIN;

BIOGENIC MN OXIDES; METAL CONTAMINATION; METAL ENRICHMENT; MINING ACTIVITIES; MN OXIDATION; SUBSURFACE LAYER; TODOROKITES; URANIUM MINING;

MANGANESE;

MANGANESE DERIVATIVE; SOIL; URANIUM;

BACTERIUM; BIOREMEDIATION; CHEMISTRY; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MINING; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PH; PHYLOGENY; SOIL;

BACTERIA; BIODEGRADATION, ENVIRONMENTAL; HYDROGEN-ION CONCENTRATION; MANGANESE COMPOUNDS; MINING; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PHYLOGENY; SOIL; SOIL MICROBIOLOGY; URANIUM;

EID: 84904861809     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01296-14     Document Type: Article

References (62)

1. 2 and Mn(II) species in aqueous solutions. Geochim. Cosmochim. Acta 69:35-48. http://dx.doi.org/10.1016/j.gca.2004.06.013.
2. Tebo BM, Bargar JR, Clement BG, Dick GJ, Murray KJ, Parker D, Verity R, Webb SM. 2004. Biogenic manganese oxides: properties and mechanisms of formation. Annu. Rev. Earth Planet. Sci. 32:287-328. http://dx.doi.org/10.1146/annurev.earth.32.101802.120213.
3. Tebo B, Clement B, Dick G. 2007. Biotransformations of manganese, p 1223-1238. In Hurst CJ (ed), Manual of environmental microbiology, 3rd ed. ASM Press, Washington, DC.
4. Geszvain K, Butterfield C, Davis R, Madison A, Lee S, Parker D, Soldatova A, Spiro T, Luther G, Tebo B. 2012. The molecular biogeochemistry of manganese(II) oxidation. Biochem. Soc. Trans. 40:1244-1248. http://dx.doi.org/10.1042/BST20120229.
5. Nealson KH. 2006. The manganese-oxidizing bacteria, p 222-231. In Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (ed), The prokaryotes. Springer, New York, NY.
6. Luther GW. 2010. The role of one-and two-electron transfer reactions in forming thermodynamically unstable intermediates as barriers in multielectron redox reactions. Aquat. Geochem. 16:395-420. http://dx.doi.org/10.1007/s10498-009-9082-3.
7. von Langen PJ, Johnson KS, Coale KH, Elrod VA. 1997. Oxidation kinetics of manganese (II) in seawater at nanomolar concentrations. Geochim. Cosmochim. Acta 61:4945-4954. http://dx.doi.org/10.1016/S0016-7037(97)00355-4.
8. Hansel C, Francis C. 2006. Coupled photochemical and enzymatic Mn(II) oxidation pathways of a planktonic Roseobacter-like bacterium. Appl. Environ. Microbiol. 72:3543-3549. http://dx.doi.org/10.1128/AEM.72.5.3543-3549.2006.
9. Francis CA, Tebo BM. 1999. Marine Bacillus spores as catalysts for oxidative precipitation and sorption of metals. J. Mol. Microbiol. Biotechnol. 1:71-78.
10. Boogerd F, de Vrind J. 1987. Manganese oxidation by Leptothrix discophora. J. Bacteriol. 169:489-484.
11. Francis CA, Tebo BM. 2001. cumA multicopper oxidase genes from diverse Mn(II)-oxidizing and non-Mn(II)-oxidizing Pseudomonas strains. Appl. Environ. Microbiol. 67:4272-4278. http://dx.doi.org/10.1128/AEM.67.9.4272-4278.2001.
12. Anderson C, Dick G, Chu M, Cho J, Davis R, Bräuer S, Tebo B. 2009. Aurantimonas manganoxydans, sp. nov. and Aurantimonas litoralis, sp. nov.: Mn(II) oxidizing representatives of a globally distributed clade of alpha-Proteobacteria from the order Rhizobiales. Geomicrobiol. J. 26:189-198. http://dx.doi.org/10.1080/01490450902724840.
13. Bromfield SM. 1979. Manganous ion oxidation at pH values below 5.0 by cell-free substances from Streptomyces sp. cultures. Soil Biol. Biochem. 11:115-118. http://dx.doi.org/10.1016/0038-0717(79)90086-5.
14. Bromfield S. 1956. Oxidation of manganese by soil microorganisms. Aust. J. Biol. Sci. 9:238-252.
15. Ivarson K, Heringa P. 1972. Oxidation of manganese by microorganisms in manganese deposits of Newfoundland soil. Can. J. Soil Sci. 52:401-416. http://dx.doi.org/10.4141/cjss72-052.
16. Sparrow LA, Uren NC. 1987. Oxidation and reduction of Mn in acidic soils: effect of temperature and soil pH. Soil Biol. Biochem. 19:143-148. http://dx.doi.org/10.1016/0038-0717(87)90073-3.
17. Learman DR, Voelker BM, Vazquez-Rodriguez AI, Hansel CM. 2011. Formation of manganese oxides by bacterially generated superoxide. Nat. Geosci. 4:95-98. http://dx.doi.org/10.1038/ngeo1055.
18. Banh A, Chavez V, Doi J, Nguyen A, Hernandez S, Ha V, Jimenez P, Espinoza F, Johnson HA. 2013. Manganese (Mn) oxidation increases intracellular Mn in Pseudomonas putida GB-1. PLoS One 8:e77835. http://dx.doi.org/10.1371/journal.pone.0077835.
19. Tebo BM, Johnson HA, McCarthy JK, Templeton AS. 2005. Geomicrobiology of manganese(II) oxidation. Trends Microbiol. 13:421-428. http://dx.doi.org/10.1016/j.tim.2005.07.009.
20. Nelson Y, Lion L, Ghiorse W, Shuler M. 1999. Production of biogenic Mn oxides by Leptothrix discophora SS-1 in a chemically defined growth medium and evaluation of their Pb adsorption characteristics. Appl. Environ. Microbiol. 65:175-180.
21. Peña J, Kwon KD, Refson K, Bargar JR, Sposito G. 2010. Mechanisms of nickel sorption by a bacteriogenic birnessite. Geochim. Cosmochim. Acta 74:3076-3089. http://dx.doi.org/10.1016/j.gca.2010.02.035.
22. Wang W, Shao Z, Liu Y, Wang G. 2009. Removal of multi-heavy metals using biogenic manganese oxides generated by a deep-sea sedimentary bacterium Brachybacterium sp. strain Mn32. Microbiology 155:1989-1996. http://dx.doi.org/10.1099/mic.0.024141-0.
23. Toner B, Manceau A, Webb S, Sposito G. 2006. Zinc sorption to biogenic hexagonal-birnessite particles within a hydrated bacterial biofilm. Geochim. Cosmochim. Acta 70:27-43. http://dx.doi.org/10.1016/j.gca.2005.08.029.
24. Burkhardt E, Meißner S, Merten D, Büchel G, Küsel K. 2009. Heavy metal retention and microbial activities in geochemical barriers formed in glacial sediments subjacent to a former uranium mining leaching heap. Chem. Erde Geochem. 69:21-34. http://dx.doi.org/10.1016/j.chemer.2008.12.003.
25. Carlsson E, Büchel G. 2005. Screening of residual contamination at a former uranium heap leaching site, Thuringia, Germany. Chem. Erde Geochem. 65:75-95. http://dx.doi.org/10.1016/j.chemer.2005.06.007.
26. Schäffner F. 2013. Natural attenuation of heavy metals in near-surface supergene Mn deposits occurring at the basement of a former leaching heap, Ronneburg, Germany. Ph.D. dissertation. Friedrich-Schiller University Jena, Jena, Germany.
27. Perel'man AI. 1967. Geochemistry of epigenesis, p 213-234. Plenum Press, New York, NY.
28. Grawunder A, Lonschinski M, Merten D. 2009. Distribution and bonding of residual contamination in glacial sediments at the former uranium mining leaching heap of Gessen/Thuringia, Germany. Chem. Erde Geochem. 69:5-19. http://dx.doi.org/10.1016/j.chemer.2008.06.001.
29. Küsel K, Ewald E-M, Sitte J. 2008. Effect of metal-reducing microorganisms on element fluxes in a former uranium-mining district, p 128-137. In Liu S-J, Drake HL (ed), Microbes in the environment: perspectives and challenges. Science Press, Beijing, China.
30. Deutsches Institut fur Normung. 2000. 19684-1:1977-02. Methods of soil analysis for water management for agricultural purposes: chemical laboratory tests; determination of pH-value of the soil and lime requirement. Handbuch der Bodenuntersuchung. Beuth Verlag, Berlin, Germany.
31. Fabisch M, Beulig F, Akob DM, Küsel K. 2013. Surprising abundance of Gallionella-related iron oxidizers in creek sediments at pH 4.4 or at high heavy metal concentrations. Front. Microbiol. 4:390. http://dx.doi.org/10.3389/fmicb.2013.00390.
32. Mulder EG, van Veen WL. 1963. Investigations on the Sphaerotilus-Leptothrix group. Antonie Van Leeuwenhoek 29:121-153.
33. Benz M, Brune A, Schink B. 1998. Anaerobic and aerobic oxidation of ferrous iron at neutral pH by chemoheterotrophic nitrate-reducing bacteria. Arch. Microbiol. 169:159-165. http://dx.doi.org/10.1007/s002030050555.
34. Krumbein W, Altmann H. 1973. A new method for the detection and enumeration of manganese oxidizing and reducing microorganisms. Helgol. Mar. Res. 25:347-356.
35. Lu S, Gischkat S, Reiche M, Akob DM, Hallberg KB, Küsel K. 2010. Ecophysiology of Fe-cycling bacteria in acidic sediments. Appl. Environ. Microbiol. 76:8174-8183. http://dx.doi.org/10.1128/AEM.01931-10.
36. Drummond A, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A. 2009. Geneious v4.6.0. Biomatters, Auckland, New Zealand.
37. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410. http://dx.doi.org/10.1016/S0022-2836(05)80360-2.
38. Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW. 2007. EzTaxon: a Web-based tool for the identification of prokaryotes based on 16S ribosomalRNAgene sequences. Int. J. Syst. Evol. Microbiol. 57:2259-2261. http://dx.doi.org/10.1099/ijs.0.64915-0.
39. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer K-H. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371. http://dx.doi.org/10.1093/nar/gkh293.
40. de Vrind JP, Boogerd FC, de Vrind-de Jong EW. 1986. Manganese reduction by a marine Bacillus species. J. Bacteriol. 167:30-34.
41. Zhou JZ, Bruns MA, Tiedje JM. 1996. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62:316-322.
42. Schloss PD, Westcott S, Ryabin T, Hall J, Hartmann M, Hollister E, Lesniewski R, Oakley B, Parks D, Robinson C, Sahl J, Stres B, Thallinger G, Van Horn D, Weber C. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541. http://dx.doi.org/10.1128/AEM.01541-09.
43. Lane DJ. 1991. 16S/23S rRNA sequencing in E. coli, p 115-175. In Stackebrandt E, Goodfellow M (ed), Nucleic acid techniques in bacterial systematics. John Wiley & Sons, New York, NY.
44. Zhou J. 2008. The development of molecular tools for the evaluation of the bioremediation of chlorinated solvents. Ph.D. dissertation. Utah State University, Logen, UT.
45. Lu S, Chourey K, Reiche M, Nietzsche S, Shah MB, Neu TR, Hettich RL, and Küsel K. 2013. Insights into the structure and metabolic function of microbes that shape pelagic iron-rich aggregates ("iron snow"). Appl. Environ. Microbiol. 79:4272-4281. http://dx.doi.org/10.1128/AEM.00467-13.
46. Löffler S. 2007. Charakterisierung der geochemischen Barrieren im Gessenbach. Ph.D. dissertation. Friedrich Schiller University Jena, Jena, Germany.
47. Finneran KT, Johnsen CV, Lovley DR. 2003. Rhodoferax ferrireducens sp. nov., a psychrotolerant, facultatively anaerobic bacterium that oxidizes acetate with the reduction of Fe(III). Int. J. Syst. Evol. Microbiol. 53:669-673. http://dx.doi.org/10.1099/ijs.0.02298-0.
48. Ramana CV, Sasikala C. 2009. Albidoferax, a new genus of Comamonadaceae and reclassification of Rhodoferax ferrireducens (Finneran et al., 2003) as Albidoferax ferrireducens comb. nov. J. Gen. Appl. Microbiol. 55:301-304. http://dx.doi.org/10.2323/jgam.55.301.
49. Takeda M, Kamagata Y, Ghiorse WC, Hanada S, Koizumi J-I. 2002. Caldimonas manganoxidans gen. nov., sp. nov., a poly(3-hydroxybutyrate)-degrading, manganese-oxidizing thermophile. Int. J. Syst. Evol. Microbiol. 52:895-900. http://dx.doi.org/10.1099/ijs.0.02027-0.
50. Lincoln SP, Fermor TR, Tindall BJ. 1999. Janthinobacterium agaricidamnosum sp. nov., a soft rot pathogen of Agaricus bisporus. Int. J. Syst. Bacteriol. 49:1577-1589. http://dx.doi.org/10.1099/00207713-49-4-1577.
51. Carmichael MJ, Carmichael SK, Santelli CM, Strom A, Bräuer SL. 2013. Mn(II)-oxidizing bacteria are abundant and environmentally relevant members of ferromanganese deposits in caves of the Upper Tennessee River Basin. Geomicrobiol. J. 30:779-800. http://dx.doi.org/10.1080/01490451.2013.769651.
52. Miyata N, Tani Y, Sakata M, Iwahori K. 2007. Microbial manganese oxide formation and interaction with toxic metal ions. J. Biosci. Bioeng. 104:1-8. http://dx.doi.org/10.1263/jbb.104.1.
53. Karelová E, Harichová J, Stojnev T, Pangallo D, Ferianc P. 2011. The isolation of heavy-metal resistant culturable bacteria and resistance determinants from a heavy-metal-contaminated site. Biologia 66:18-26. http://dx.doi.org/10.2478/s11756-010-0145-0.
54. Mera N, Iwasaki K. 2007. Use of plate-wash samples to monitor the fates of culturable bacteria in mercury-and trichloroethylene-contaminated soils. Appl. Microbiol. Biotechnol. 77:437-445. http://dx.doi.org/10.1007/s00253-007-1152-0.
55. Margesin R, Schinner F. 1996. Bacterial heavy metal-tolerance-extreme resistance to nickel in Arthrobacter spp. strains. J. Basic Microbiol. 36:269-282. http://dx.doi.org/10.1002/jobm.3620360410.
56. Benyehuda G, Coombs J, Ward PL, Balkwill D, Barkay T. 2003. Metal resistance among aerobic chemoheterotrophic bacteria from the deep terrestrial subsurface. Can. J. Microbiol. 49:151-156. http://dx.doi.org/10.1139/w03-012.
57. Abou-Shanab RA, van Berkum P, Angle JS. 2007. Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere 68:360-367. http://dx.doi.org/10.1016/j.chemosphere.2006.12.051.
58. Kosman D. 2010. Multicopper oxidases: a workshop on copper coordination chemistry, electron transfer, and metallophysiology. J. Biol. Inorg. Chem. 15:15-28. http://dx.doi.org/10.1007/s00775-009-0590-9.
59. Junta JL, Hochella MF, Jr. 1994. Manganese(II) oxidation at mineral surfaces: a microscopic and spectroscopic study. Geochim. Cosmochim. Acta 58:4985-4999. http://dx.doi.org/10.1016/0016-7037(94)90226-7.
60. Parker DL, Sposito G, Tebo BM. 2004. Manganese(III) binding to a pyoverdine siderophore produced by a manganese(II)-oxidizing bacterium. Geochim. Cosmochim. Acta 68:4809-4820. http://dx.doi.org/10.1016/j.gca.2004.05.038.
61. 2 precipitation, siderophore-Mn(III) complex formation, siderophore degradation, and iron limitation in Mn(II)-oxidizing bacterial cultures. Geochim. Cosmochim. Acta 71: 5672-5683. http://dx.doi.org/10.1016/j.gca.2007.03.042.
62. Diaz JM, Hansel CM, Voelker BM, Mendes CM, Andeer PF, Zhang T. 2013. Widespread production of extracellular superoxide by heterotrophic bacteria. Science 340:1223-1226. http://dx.doi.org/10.1126/science.1237331.